Fecal microbiota transplantation modulates jejunal host-microbiota interface in weanling piglets

Abstract Background Weaning-associated enteric diseases are a major concern in the swine industry. This study investigates the effects of fecal microbiota transplantation (FMT) on the jejunum of weanling piglets, a segment of bowel less studied in terms of microbiomic changes despite its primary inv...

Full description

Saved in:
Bibliographic Details
Main Authors: Shankumar Mooyottu, Muhammed Shafeekh Muyyarikkandy, Farnaz Yousefi, Ganwu Li, Orhan Sahin, Eric Burrough, Joy Scaria, Brett Sponseller, Alejandro Ramirez
Format: Article
Language:English
Published: BMC 2025-02-01
Series:Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40168-025-02042-9
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1823861800554201088
author Shankumar Mooyottu
Muhammed Shafeekh Muyyarikkandy
Farnaz Yousefi
Ganwu Li
Orhan Sahin
Eric Burrough
Joy Scaria
Brett Sponseller
Alejandro Ramirez
author_facet Shankumar Mooyottu
Muhammed Shafeekh Muyyarikkandy
Farnaz Yousefi
Ganwu Li
Orhan Sahin
Eric Burrough
Joy Scaria
Brett Sponseller
Alejandro Ramirez
author_sort Shankumar Mooyottu
collection DOAJ
description Abstract Background Weaning-associated enteric diseases are a major concern in the swine industry. This study investigates the effects of fecal microbiota transplantation (FMT) on the jejunum of weanling piglets, a segment of bowel less studied in terms of microbiomic changes despite its primary involvement in major post-weaning enteric diseases, including postweaning diarrhea (PWD). Thirty-two 3-week-old piglets were divided equally into two groups: Control and FMT. The FMT group received fecal microbiota preparation from 3-month-old healthy pigs on the 1st and 3rd day after weaning. Half of each group was inoculated with an enterotoxigenic E. coli (ETEC) isolate 10 days post-FMT. Piglets were euthanized in the third week (14th and 18th days post-FMT) after weaning to collect intestinal tissues and contents for microbiomic, metabolomic, and transcriptomic analyses. Results The jejunal microbiota showed a significant increase in alpha diversity in the third week post-FMT compared with the ileum and colon. FMT significantly enriched the jejunal microbiota composition, while multiple bacterial genera were specifically lacking in control weanling piglets. FMT was strongly associated with the enrichment of the genus Pseudoscardovia of the Bifidobacteriaceae family, which was found lacking in the jejunum of weanling control piglets and inversely associated with the abundance of the genus Bifidobacterium within the same family. Other genera associated with FMT included Solobacterium, Shuttleworthia, and Pseudoraminibacter, whereas bacteria such as Erysipelotrichaceae and Acidaminococcus were identified as most abundant in the control piglets. Metabolomic analysis revealed a significant modulatory effect of FMT on carbohydrate, amino acid, nucleotide, vitamin, and xenobiotic metabolisms, suggesting improved nutrient utilization. Transcriptomic analyses further confirmed the regulatory effects of FMT on gene expression associated with immune, metabolic, barrier, and neuroendocrine functions. Prior FMT treatment in the context of ETEC infection indicated a potential protective role, as evidenced by a significant shift in microbial diversity and metabolomic compositions and decreased diarrhea severity even though no effect on pathogen shedding was evident. Conclusions This study underscores the promise of FMT in enhancing jejunal health. In addition, the results suggest that FMT could be considered a potential strategy to address conditions associated with small intestinal dysbiosis in swine and other monogastric species with similar gut anatomy and physiology, such as humans. Video Abstract
format Article
id doaj-art-4cae3860ffbc452fab66bc88a31b22f5
institution Kabale University
issn 2049-2618
language English
publishDate 2025-02-01
publisher BMC
record_format Article
series Microbiome
spelling doaj-art-4cae3860ffbc452fab66bc88a31b22f52025-02-09T12:46:47ZengBMCMicrobiome2049-26182025-02-0113112410.1186/s40168-025-02042-9Fecal microbiota transplantation modulates jejunal host-microbiota interface in weanling pigletsShankumar Mooyottu0Muhammed Shafeekh Muyyarikkandy1Farnaz Yousefi2Ganwu Li3Orhan Sahin4Eric Burrough5Joy Scaria6Brett Sponseller7Alejandro Ramirez8Auburn UniversityUniversity of DelawareAuburn UniversityIowa State UniversityIowa State UniversityIowa State UniversityOklahoma State UniversityIowa State UniversityIowa State UniversityAbstract Background Weaning-associated enteric diseases are a major concern in the swine industry. This study investigates the effects of fecal microbiota transplantation (FMT) on the jejunum of weanling piglets, a segment of bowel less studied in terms of microbiomic changes despite its primary involvement in major post-weaning enteric diseases, including postweaning diarrhea (PWD). Thirty-two 3-week-old piglets were divided equally into two groups: Control and FMT. The FMT group received fecal microbiota preparation from 3-month-old healthy pigs on the 1st and 3rd day after weaning. Half of each group was inoculated with an enterotoxigenic E. coli (ETEC) isolate 10 days post-FMT. Piglets were euthanized in the third week (14th and 18th days post-FMT) after weaning to collect intestinal tissues and contents for microbiomic, metabolomic, and transcriptomic analyses. Results The jejunal microbiota showed a significant increase in alpha diversity in the third week post-FMT compared with the ileum and colon. FMT significantly enriched the jejunal microbiota composition, while multiple bacterial genera were specifically lacking in control weanling piglets. FMT was strongly associated with the enrichment of the genus Pseudoscardovia of the Bifidobacteriaceae family, which was found lacking in the jejunum of weanling control piglets and inversely associated with the abundance of the genus Bifidobacterium within the same family. Other genera associated with FMT included Solobacterium, Shuttleworthia, and Pseudoraminibacter, whereas bacteria such as Erysipelotrichaceae and Acidaminococcus were identified as most abundant in the control piglets. Metabolomic analysis revealed a significant modulatory effect of FMT on carbohydrate, amino acid, nucleotide, vitamin, and xenobiotic metabolisms, suggesting improved nutrient utilization. Transcriptomic analyses further confirmed the regulatory effects of FMT on gene expression associated with immune, metabolic, barrier, and neuroendocrine functions. Prior FMT treatment in the context of ETEC infection indicated a potential protective role, as evidenced by a significant shift in microbial diversity and metabolomic compositions and decreased diarrhea severity even though no effect on pathogen shedding was evident. Conclusions This study underscores the promise of FMT in enhancing jejunal health. In addition, the results suggest that FMT could be considered a potential strategy to address conditions associated with small intestinal dysbiosis in swine and other monogastric species with similar gut anatomy and physiology, such as humans. Video Abstracthttps://doi.org/10.1186/s40168-025-02042-9Postweaning diarrheaFecal microbiota transplantationWeanling piglets
spellingShingle Shankumar Mooyottu
Muhammed Shafeekh Muyyarikkandy
Farnaz Yousefi
Ganwu Li
Orhan Sahin
Eric Burrough
Joy Scaria
Brett Sponseller
Alejandro Ramirez
Fecal microbiota transplantation modulates jejunal host-microbiota interface in weanling piglets
Microbiome
Postweaning diarrhea
Fecal microbiota transplantation
Weanling piglets
title Fecal microbiota transplantation modulates jejunal host-microbiota interface in weanling piglets
title_full Fecal microbiota transplantation modulates jejunal host-microbiota interface in weanling piglets
title_fullStr Fecal microbiota transplantation modulates jejunal host-microbiota interface in weanling piglets
title_full_unstemmed Fecal microbiota transplantation modulates jejunal host-microbiota interface in weanling piglets
title_short Fecal microbiota transplantation modulates jejunal host-microbiota interface in weanling piglets
title_sort fecal microbiota transplantation modulates jejunal host microbiota interface in weanling piglets
topic Postweaning diarrhea
Fecal microbiota transplantation
Weanling piglets
url https://doi.org/10.1186/s40168-025-02042-9
work_keys_str_mv AT shankumarmooyottu fecalmicrobiotatransplantationmodulatesjejunalhostmicrobiotainterfaceinweanlingpiglets
AT muhammedshafeekhmuyyarikkandy fecalmicrobiotatransplantationmodulatesjejunalhostmicrobiotainterfaceinweanlingpiglets
AT farnazyousefi fecalmicrobiotatransplantationmodulatesjejunalhostmicrobiotainterfaceinweanlingpiglets
AT ganwuli fecalmicrobiotatransplantationmodulatesjejunalhostmicrobiotainterfaceinweanlingpiglets
AT orhansahin fecalmicrobiotatransplantationmodulatesjejunalhostmicrobiotainterfaceinweanlingpiglets
AT ericburrough fecalmicrobiotatransplantationmodulatesjejunalhostmicrobiotainterfaceinweanlingpiglets
AT joyscaria fecalmicrobiotatransplantationmodulatesjejunalhostmicrobiotainterfaceinweanlingpiglets
AT brettsponseller fecalmicrobiotatransplantationmodulatesjejunalhostmicrobiotainterfaceinweanlingpiglets
AT alejandroramirez fecalmicrobiotatransplantationmodulatesjejunalhostmicrobiotainterfaceinweanlingpiglets